Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2022 Aug;103(8):e3685.
doi: 10.1002/ecy.3685. Epub 2022 Jun 14.

Temperature impacts the environmental suitability for malaria transmission by Anopheles gambiae and Anopheles stephensi

Affiliations

Temperature impacts the environmental suitability for malaria transmission by Anopheles gambiae and Anopheles stephensi

Oswaldo C Villena et al. Ecology. 2022 Aug.

Abstract

Extrinsic environmental factors influence the spatiotemporal dynamics of many organisms, including insects that transmit the pathogens responsible for vector-borne diseases (VBDs). Temperature is an especially important constraint on the fitness of a wide variety of ectothermic insects. A mechanistic understanding of how temperature impacts traits of ectotherms, and thus the distribution of ectotherms and vector-borne infections, is key to predicting the consequences of climate change on transmission of VBDs like malaria. However, the response of transmission to temperature and other drivers is complex, as thermal traits of ectotherms are typically nonlinear, and they interact to determine transmission constraints. In this study, we assess and compare the effect of temperature on the transmission of two malaria parasites, Plasmodium falciparum and Plasmodium vivax, by two malaria vector species, Anopheles gambiae and Anopheles stephensi. We model the nonlinear responses of temperature dependent mosquito and parasite traits (mosquito development rate, bite rate, fecundity, proportion of eggs surviving to adulthood, vector competence, mortality rate, and parasite development rate) and incorporate these traits into a suitability metric based on a model for the basic reproductive number across temperatures. Our model predicts that the optimum temperature for transmission suitability is similar for the four mosquito-parasite combinations assessed in this study, but may differ at the thermal limits. More specifically, we found significant differences in the upper thermal limit between parasites spread by the same mosquito (A. stephensi) and between mosquitoes carrying P. falciparum. In contrast, at the lower thermal limit the significant differences were primarily between the mosquito species that both carried the same pathogen (e.g., A. stephensi and A. gambiae both with P. falciparum). Using prevalence data, we show that the transmission suitability metric ST$$ S(T) $$ calculated from our mechanistic model is consistent with observed P. falciparum prevalence in Africa and Asia but is equivocal for P. vivax prevalence in Asia, and inconsistent with P. vivax prevalence in Africa. We mapped risk to illustrate the number of months various areas in Africa and Asia predicted to be suitable for malaria transmission based on this suitability metric. This mapping provides spatially explicit predictions for suitability and transmission risk.

Keywords: Africa; Asia; Plasmodium falciparum; Plasmodium vivax; basic reproductive number; malaria; mosquito life history; thermal performance curve; vector-borne diseases.

PubMed Disclaimer

Conflict of interest statement

The authors declare no conflict of interest.

Figures

FIGURE 1
FIGURE 1
Posterior mean (solid line) and 95% highest posterior density (HPD; dashed lines) of the thermal responses for mosquito traits for Anopheles stephensi (green) and Anopheles gambiae (blue). Traits modeled with a Brière thermal response are (a, f) mosquito development rate and (b, g) bite rate. Traits modeled with a concave down quadratic function are (c, h) proportion of eggs surviving to adulthood and (d, i) fecundity and (e, j) mortality rate, which is modeled with a concave‐up quadratic function. Data symbols correspond to the species of mosquitoes. Open circles, A. stephensi; solid circles, A. gambiae; crosses, A. arabiensis; stars, A. pseudopunctipennis. For parasites and compound traits (mosquitoes + parasites), see Appendix S1
FIGURE 2
FIGURE 2
Top row: relative transmission suitability ST divided by the maximum value of the posterior median for (a) A. stephensi/Plasmodium falciparum, (b) A. stephensi/Plasmodium vivax, (c) A. gambiae/P. falciparum, and (d) A. gambiae/P. vivax. Bottom row: median, interquartile range, minimum, and maximum numbers from the posterior for the minimum temperature, optimum temperature, and maximum temperature for the ST of (e) A. stephensi/P. falciparum, (f) A. stephensi/P. vivax, (g) A. gambiae/P. falciparum, and (h) A. gambiae/P. vivax
FIGURE 3
FIGURE 3
The number of months a year that locations fall within the predicted suitable range (probability of ST > 0 0.975) for the transmission of Plasmodium falciparum by (a) Anopheles stephensi and (b) Anopheles gambiae mosquitoes in Africa, and for the transmission of (c) P. falciparum and (d) Plasmodium vivax by A. stephensi mosquitoes in Asia

Similar articles

Cited by

References

    1. Abram, P. K. , Boivin G., Moiroux J., and Brodeur J.. 2017. “Behavioural Effects of Temperature on Ectothermic Animals: Unifying Thermal Physiology and Behavioural Plasticity.” Biological Reviews 92: 1859–76. - PubMed
    1. Aho, K. , Derryberry D., and Peterson T.. 2014. “Model Selection for Ecologists: The Worldviews of AIC and BIC.” Ecology 95: 631–6. - PubMed
    1. Amarasekare, P. , and Savage V.. 2012. “A Framework for Elucidating the Temperature Dependence of Fitness.” The American Naturalist 179: 178–91. - PubMed
    1. Balk, D. L. , Deichmann U., Yetman G., Pozzi F., Hay S. I., and Nelson A.. 2006. “Determining Global Population Distribution: Methods, Applications and Data.” Advances in Parasitology 62: 119–56. - PMC - PubMed
    1. Balkew, M. , Mumba P., Dengela D., Yohannes G., Getachew D., Yared S., Chibsa S., et al. 2020. “Geographical Distribution of Anopheles stephensi in Eastern Ethiopia.” Parasites & Vectors 13: 35. 10.1186/s13071-020-3904-y - DOI - PMC - PubMed

Publication types

LinkOut - more resources